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An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos

Nature Cell Biology volume 12, pages 60–65 (2010)Cite this article

Abstract

Partitioning tissues into compartments that do not intermix is essential for the correct morphogenesis of animal embryos and organs1,2,3. Several hypotheses have been proposed to explain compartmental cell sorting, mainly differential adhesion1,2,3,4,5,6,7,8,9, but also regulation of the cytoskeleton10,11 or of cell proliferation10,12. Nevertheless, the molecular and cellular mechanisms that keep cells apart at boundaries remain unclear. Here we demonstrate, in early Drosophila melanogaster embryos, that actomyosin-based barriers stop cells from invading neighbouring compartments. Our analysis shows that cells can transiently invade neighbouring compartments, especially when they divide, but are then pushed back into their compartment of origin. Actomyosin cytoskeletal components are enriched at compartmental boundaries, forming cable-like structures when the epidermis is mitotically active. When MyoII (non-muscle myosin II) function is inhibited, including locally at the cable by chromophore-assisted laser inactivation (CALI)13,14, in live embryos, dividing cells are no longer pushed back, leading to compartmental cell mixing. We propose that local regulation of actomyosin contractibility, rather than differential adhesion, is the primary mechanism sorting cells at compartmental boundaries.

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Figure 1: Myosin II is required for cell sorting at lineage restriction boundaries in Drosophila embryos.
Figure 2: An actomyosin cable forms at the PS boundary.
Figure 3: Cell divisions challenge PS boundaries.
Figure 4: CALI inactivation of MyoII blocks cytokinesis.
Figure 5: CALI inactivation of the MyoII cable causes cell sorting defects at PS boundaries.

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Acknowledgements

We thank N. Lawrence for the initial observation of the segmental pattern of MyoII cables and for Supplementary Information, Movie 1; B. Bordbar for help in screening chromosomal deficiencies; D. Kiehart, R. Karess, G. Davis, J. Pradel, R. Holmgren, the UK Protein Trap Insertion Consortium, the Bloomington Stock Centre and the Developmental Studies Hybridoma Bank for reagents and B. Harris, R. Keynes, L. Perrin, M. Sémériva and D. St Johnston for critical reading of the manuscript. This work was funded by HFSP and Wellcome Trust grants to B.S; a Wellcome Trust Program Grant to A.H.B; an EMBO fellowship to A.P-M and ARC (Association pour la Recherche contre le Cancer) and Herchel Smith fellowships to B.M.

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  1. Bruno Monier and Anne Pélissier-Monier: These authors contributed equally to the work.

Authors and Affiliations

  1. Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge, CB2 3DY, UK

    Bruno Monier, Anne Pélissier-Monier, Andrea H. Brand & Bénédicte Sanson

  2. The Gurdon Institute, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QN, UK

    Anne Pélissier-Monier & Andrea H. Brand

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Experimental work and data analysis were carried out by A.P-M and B.M. under supervision of A.H.B. and B.S. All authors contributed to data interpretation and writing of the manuscript.

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Correspondence to Bruno Monier or Bénédicte Sanson.

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Monier, B., Pélissier-Monier, A., Brand, A. et al. An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos. Nat Cell Biol 12, 60–65 (2010). https://doi.org/10.1038/ncb2005

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